Intemational JoumaJ 01 Primalology, Vol. 14, No. 3, 1993
Sleeping Sites and Lodge Trees of the Night Monkey (Aotus azarae) in Bolivia
Juan E. Garcial and Francisco Brazal Received June 21, 1990,. accepled January 7, 1992
Between 1984 and 1987, we recorded the sleeping-site and lodge tree preferenees of night monkeys at the Beni Biologieal Station, Bolivia. We eharaeterized the strueture of sleeping-site compared lodge trees to nonlodge trees, and determined the frequency of their use. Aotus azarae used braneh and liana platforms on trees of the middle strata of the forest as sleeping sites, but the lodge trees provided sparse caver. Monkeys may manipulate either natural aecumulations of material or bird nests to serve as sleeping sites. The eharaeteristies of the sleeping site and of the Iodge trees may be related to proteetion against predators and to thermal advantages. The distribution of lodge trees appeared to be re/ated to aeeess to food. Aetivities around the sleeping site eould be re/ated to marking behavior. KEY WORDS: Aolus azarae,. behavioral ecology; sleeping siles; lodge lrccs; marking bchavior.
INTRODUCTION
Sleeping sites have been doeumented for sorne neotropieal primates of the genera Callieebus (Kinzey, 1981; Kinzey et al., 1977; Mason, 1966, 1968), Leonthopiteeus (Coimbra-Filho, 1977), and Alouatta (Braza, 1980). Night monkeys (Aotus spp.) are repoTled to sleep in tree holes (Napier and Napier, 1967; Thorington et al., 1976; Hershkovitz, 1983; Aquino and Encarnacion, 1986, 1992) and to sleep on frameworks of branches and li anas (Thorington et al., 1976; Rathbun and Gache, 1977; Wright, 1978, 1981, 1983; Hershkovitz, 1983; Garcia, 1988). We provide data about night monkeys sleeping si tes, describe their structura! characteristics, and com lEslacion Biologica de Doñana, Aparlado 1056, 41080 Sevilla, Spain.
467
OI64·0291I'J3106OO-0467S07.00I0 o 1993 Plenum PuDli.shlng Corporation 468 Garda and Bram pare sleeping with nonsleeping sites and lodge trees with nonlodge trees in order to evaluate the functional basis for their microhabitat preferences.
STUOY AREA ANO METHOOS
The study area is =135,000 ha of the Beni Biological Station, in the Department Beni, Bolivia (66°18'30"W, 14°38'00"S), which is at an =270-m altitude. The area is part of the Llanos de Moxos, which are among the largest flooded neotropical savannas. The area is markedly seasonal, with a rainy season from November to May (summer) and a dry season from June to September (winter). Data from the village of San Borja 50 km from our observation area, show that, during the study period, the mean maximum temperature in the rainy season was 30°C and the mean mini mum temperature was 22°C (range variation from 20 to 34°C). During the dry season the mean maximum temperature was 28°C and the mean mini mum temperature was 18°C (range, 8-31°C), with differences reaching 15°C between the maximum and the minimum daily temperatures. For 3- to 5 day periods during the dry season ambient temperatures were ~6°C for the locality of Espiritu (Beck, 1984), depending on the strength of cool pre vailing winds from the south. These periods are locally known as surazos. The average annual precipitation is 1450 mm. The vegetation of the area ineludes tropical and subtropical evergreen seasonal lowland forest (Ellen berg and Mueller-Dombois, 1965) and island forest and gallery forest (Liberman, 1985); =10% of the area is an open savannah. We identified the sleeping si tes of approximately six groups of mon keys and studied two groups intensively. Data on their use of space and activity panerns are published (Garcia, 1988; Garcia and Braza, 1987). Group 1 inhabited island forest, corresponding with the type defined as "island linle altered" by Beck (1984), with macrophanerophites, ineluding Ficus ob/usiuscula, Capai/era reticulata, Guazuma u/mi/oUa, pairo trees (Scheelea prineeps), and thickets of Genipa americana and Rheedia spp. Group 2 inhabited a low riverine forest characterized by tropical species subject to seasonal inundation from December to May. The most common tree species are piraquina (Xylopia sp.), aehachairu (Rheedia sp.), bibosi (Fieus sp.), paeai (Tnga sp.), and chonta (Astrocaryum chonta), and the un derstory ineludes lianas - uña de gato (Maefadena unqui-eat) and other Bignonaceae - in abundance. We observed possible sleeping sites and lodge trees in island forest and gallery fores!. We observed the subjects from down to dusk during moonlit nights. We rarely used artificial light since the monkeys' outlines were e1early visible against the sky. We also located family groups and SleeplnK Sltes and Lodge Trees or the NIKht Monkey 469 sleeping si tes via direct visual contact at twilight and predawn census. If monkeys used a site, we noted the species of tree in which the sleeping site was located (Iodge tree), its height, and the structure of the forest in its immediate vicinity. We recorded aloo its structural characteristics and the posilion of the site in the lodge tree (height, distance between the sleep ing site and the tip of the longest horizontal bough, and site to central trunk distance). We conducted more detailed observations on the structure and material used to construct sleeping sites by group 1 (n = 5 sites) and group 2 (n = 3 si tes) and their location in the groups' home ranges. In order to estimate the nature of a preference, we compared the habitat features around each lodge tree used by our two main study groups with those around each of 47 randomly selected points in the groups home range. We measured nine variables. In four 10 x lO-m quadrants, defined about each randomly selected point or lodge tree, we counted (variable 1) the number of trees and the number of lianas (variable 2). We noted the tree which was next to the randomly selected point in each quadrant and recorded the maximum distance from one of the four trees to the randomly selected point (variable 3) and the minimum distance (variable 4); the maxi mum perimeter of the four trees (variable 5) and the minimum perimeter (variable 6); and the maximum height among the four trees (variable 7) and the minimum height (variable 8). FinaHy, we measured cover as the proportion of ground occupied by perpendicular projection of the aerial parts of the trees on the ground (variable 9) (Greig-Smith, 1980; cited by Mateucci and Colma, 1982). We measured aH variables in meters and em ployed stepwise discriminant analysis (Oixon, 1975, 1981). On 59 nights, we measured the time between commencement of ac tivity at the sleeping si te and leaving the sleeping site (TA) at dusk. On 44 occasions we measured the period between entering the sleeping site and the time activity ceased (TO). 'o"
RESULTS
found 16 sleeping sites, which consisted of thickets of branches lianas that formed compact support platforms <2 m in diameter. One of them was composed of bamboo (Arundo donax). They also occa . sionaÜy rested during the daytime on exposed branches, which are excluded from our analyses due to their infrequent use and different fundian: The lodge trees, where the sleeping sites are located, were in ihe. middle stratum of the forest, the mean height of which is 12.8 m (n = 15, SO = 2.7). The mean height of the sleeping sites is 10.8 (n = 13, SO = 2.7); they were situated on the main axis of the tree, with a mean 470 Gllrcia and Braza
distance of 0.9 m (n = 13, SD = 1.1) from the central trunk and 1-4 m from the tip of the longest horizontal bough of the lodge tree (n = 13, SD = 0.9). The sleeping sites were always located among branches with a diameter $10 cm, and never at the top of a tree. We always found one sleeping site in each lodge tree.
Selection of the Lodge Tree
Table 1 lists mean values and standard deviations for eaeh of the nine variables that we measured on the 8 lodge trees of our study groups and on 47 randomly seleeted trees. Lodge trees exhibit signifieantly less eover and more lianas than those in the general habitat (F = 17, 28, gl = 3, 47, P < 0.01, stepwise discriminant analysis). Tbe eight lodge trees are situated <10 m from the edge of the island forest (group 1) and a stream (group 2) (Figs. 1 and 2).
Utilization of the Sleeping Sites and Lodge Trees
Figure 3 shows the frequeney of use of eaeh group's sleeping sites. In both cases, sorne sleeping sites were used more frequently than oth ers (X' = 22.406, gl = 4, and X' = 27.486, gl = 2, P < 0.01, respeetively). Further, we analyzed how often the sleeping sites were ehanged. We eonsidered 34 pairs of days for group 1 and 39 pairs for group 2. Group 1 always slept in the same site during the dry season, but they ehanged sleeping sites on 50% of oeeasions during the rainy season. Group 2 ehanged sleeping sites eaeh night during the dry sea son (X' = 11.266, gl = 1, P < 0.01), while during the rainy season, 'they slept in the same place on eonseeutive days (X' = 10.666, gl = 1. .p.<.,p:Ol).
•,: 'Activities of the Monkeys Around the Sleeping Sites 'íl.. .. '.~ :".[.,:' :~'"
, 00 Eaeh of the eight lodge trees of the two study groups had between ·.,,~.o~
~'" • •... ~ ~ Table l. Means and Standard Oeviations of the Nine Variables Measured in lhe Habitat and Lodge Teees
tcee Lodge ~ Lodge teees Habitat and habitat • !<, ;. Variable X SO X SO X SO • z 1. No. of teees 39.00 20.15 43.87 7.59 43.49 8.89 ;; 2. No. of lianas 22.25 20.12 13.32 8.55 14.02 9.66 ¡¡: 3. Majar dislance 17.62 28.28 5.75 1.47 6.88 7.14 4. Minar dislance \.20 0.45 2.16 0.49 2.09 0.92 ~ 5. Majar perimeler 1.00 0.36 0.97 0.53 0.97 0.52 6. Minar perimeter 0.33 0.19 0.27 0.10 0.27 0.10 ! 7. Majar height 12.75 1.19 15.30 5.71 15.09 5.54 8. Minar height 7.25 3.12 5.05 1.72 5.22 184 9. Cover 16.47 19.18 34.50 3.32 33.05 5.73 n 8 47 55
!l ~ 471 Garcia and Braza
GROUP 1
• steeping sfte _ home range - Island tore-st
15m
Fig. ]. Group 1 sleepíng siles/lodge trees in lhe isJand foresL.
GROUP 2
• sleeplng sb _ home raflge
DJ •
"""' slream
50m
Fig. 1. Group 2 sleeping silesllodge trees in lhe )ow river foresto Sleeplng SUes snd Lodge Trees of the N(gh1 Monkey 473
GrOup 1
slooplng slles
Oroup 2 30 I N"
." U '" j ,•e I .. I .t:• '" j I • - 01 03
Fig. 3. Frequency of use of each group's sleeping sites,
.' juveniles are common. Normally urination was the first activity that we .,dé.tectéd. .'h'!;'·· On average, group 1 took 7.6 ± 4.8 min to ¡eave the sleeping site .' (TA) and 3.8 ± 4.8 min (ID) to cease activities in the morning; the dif ference is significant (U = 144, P < 0.01, Mann-Whitney test). Group 2 . showed a similar pattern (TA = 14.6 ± 12.2 min; TD=1.54 ± 2.6 min; U ::,;'= 39, P < 0.01, Mann-Whitney test). There was no significant difference " ~etween TA and TD during either season (U = 19, ns, Mann-Whitney :. test), and no significant difference between TA and ID in either groups '~(l.l ;= 46.5, ns, Mann-Whitney test). :"~~!~t· , ji;:,' 474 Garclu IInd Braza
DISCUSSION
Although night monkeys do not build nests like those of gorillas (Sehaller, 1964) and ehimpanzees (Lawiek-Goodall, 1971), they c1early pre fer eertain plaees to sleep during the day and to take refuge during the night in seleet loeations, particularly thickets, dense foliage, and lianas. The disposition of the branehes and lianas at their sleeping sites is unlikely to have been produeed by ehanee. Rathbun and Gaehe (1980) indieate that, although Aotus may use these kinds of struetures in Argentina, they are skeptical that they aetually build them. We did not observe nest building or nest material modifieation but it is possible that the subjeets manipulated either natural aeeumulations of material or old bird nests for their own use. The use of sleeping siles over several years (Garcia, 1988) suggests that Aotlls at least eonduet repairs, which suggests building eapacity. The seleetion of platforms as sleeping sites in lodge trees wilh plen tiful lianas eould proteet them against diurnal predators, including Spuaetus, Harpyhalie/us, Fe/is parda/is, and probably Eira barbara. We never observed Aotus azarae sleeping in holes of trees, unlike A. naneymai and A. vociferans (Hershkovitz, 1983; Aquino and Enearnaeion, manuseript). The seleetion of platforms in lodge trees with poor eover suggests that their choice eonfers an advantage by permitting the monkeys to sun bathe on branehes near the sleeping site. Wright (1983) indicates that, in Paraguay, Aotus oeeasionally sleep on open branehes during the day. We observed this oeeasionally during June and July, when it was sunny. Tem peratures during these months have been reeorded as ~8°C at San Borja and 6°C at Espiritu (Beek, 1984), when notable winds also were observed. At 10'C and 5-m/see windspeed, environmental eooling power >600 keal/m hr (Terjung, 1966), but under eonditions of bright sunshine, eooling is re dueed =200 keal/m hr (Terjung, 1966). The resultant cooling effeet may well be redueed to =400 keal/m hr by sunbathing, and the resting position funetions to gain an energetic advantage, like that of maeaques (Dahl and Smith, 1985; Dahl et al., 1986). Aeeordingly, night monkeys that rest on open branehes during sunny days might reduce this eooling effeet. With respeet to the frequency of use and ehanges of sleeping sites, Beni night monkeys used fewer fixed lodge trees than other populations do. Wright (1978, 1983) indieated that, in Peru, A. /rivirgatus use 3-5 lodge trees, and in Paraguay, monkeys use ,,42 different lodge trees (Wright, 1982). At Beni, individuals of group 2, whieh oeeupy a low riverine forest with a mueh larger home range and whose movements are more erratic during the dry season (Gareia, 1988), use different sleeping sites. This seems to facilitate their loeation of food. But, during the rainy season, when Sleeplng SUes and Lodge Trees oC .he Nlght Monkey 475 resources are more abundanI, lhey use sleeping siles in a manner lhal fa cililales use of food lrees via flXed well-known palhways (Garcia, 1988). We suggesl lhal lhe use of lodge lrees and sleeping siles is relaled mainty lo food availability, bul new dala are necessary lo confirm lhis point. Group 1 uses lhe same sleeping sile during lhe dry season and several sleeping siles during lhe rainy season; lhis may be relaled lo varialion of slruclural characlerislics of lhe habilat. In lhe istand foresl, wilh a smaller home range, lhere musl be fewer slruclures, like bird nesls or nalural ac cumutalions of branches, which lhe monkeys can use lo sleep on, and lhe dislance between fruiling lrees musl be smaller. Finally, lhe lime when lhey exil lheir sleeping siles depends on main lenance and probably also marking aclivilies. Although ,.le did nol observe lhe monkeys marking branches with urine or anal rubbing, wilh a possible lerritorial funclion (Wrighl, 1981), one of lhe firsl aclivilies lhal we re· corded is urinalion, which is consislent wilh marking. The funclion of lhese aclivilies could be eilher inlerlroop lerrilorial defense, like Alaualla seni culus (Braza e/ al., 1981), merely lO ensure lheir own range recognition.
CONCLUSION
1. Nighl monkeys, Aa/us azarae baliviensis, use few sleeping siles, which consist of branches and lianas lhal form plalforms in lodge lrees wilh abundanI lianas and liule cover around. 2. We did not observe lhem lo build, modify, repair nesls, bul sorne modificalions of nalural accumulalions of malerial or of bird nesls is likely because similar slruclures did not appear elsewhere in lheir home ranges. 3. Abundanl lianas around the sleeping sile protecl againsl predalors, and lilUe cover around lhe lodge tree could confer a crilical lhermal ad vanlage. 4. Dislribulion and use of lodge lrees can be relaled mainly to food availability and slruclural characlerislics oC the habilat. 5. The delay in leaving sleeping siles al dusk conlribules lo mainle nance aClivity and could have a marking funclion.
ACKNOWLEDGMENTS
We lhank lhe Eslacion Biologica Beni for making our sludies possi ble. We were supporled by a granl from lhe Minislerio de Asunlos Exteriores of Spain. Vicenle Caslello conlribuled lo lhe slalislical analysis. We especially wish lo thank Tilo Zelada for his knowledge of lhe area and his valuable assislance. 476 Garcia and Braza REFERENCES
Aquino, R., and Encamacion, F. (1986). Population structure of AQtus nancymai (Cebidae: Primates) in Peruvian Amazon lowland foresto Am. J. Primalol. 11(1): 1-7. Aquino. R., and Encarnacion, F. (1992). Characteristics and use of sleeping sites in Aotus (Cebidae: Primates) in the Amazonian lowlands oC Pero (in press). Beck, S. G. (J984). Comunidades vegetales de las sabanas inundadizas en el NE lhe Bolivia. Phytocoenologia ]2(2/3): 321-350. Braza, F. (1980). El Araguato rojo (Alouatta seniculus), Doñana Acta Vertebrata, Vol. 7-5, special numo thcsis. Braza, F., Alvarez, F., and Azcarate. T. (1981). Behavior oí the red howler monkey (Alouatta seniculus) in the llanos oC Venezuela. Primates 22(4): 459-473. Coimbra-Filho, A. F. (1977). Natural shelters of Leontopithecus rasalia and sorne ecological implications (Callitrichidae: Primates). In Klciman, D. G. (ed.), Biology and Conservation 01 the CaJlitrichidae, Smithsonian Institution Press, WashingLon, D.C., pp. 79-89. Dahl, J. F., and Smith, E. O. (1985). Assessing variation in the social behavior of Stumptail macaques using thermal criteria. Am. J. Phys. AnlhropoL 68: 467-477. Dahl, J. F., Bernstein, l. S., and Williams, L. E. (1986). Thermoregulation and social sLructure of a captive group oC Rhesus Macaques. In Taubf, D. M., and King, F. A. (eds.), Cumnt Perspectil/es in Primate Social Dynamics, Van NosLrand Reinhold, New York, pp. 243-251. D~on, W. J. (1975). BMDP Biomedical Computa Programs, University oC California Press, Berkeley. D~on, W. J. (1981). BMDP Slatistical Software, University of California Press, Berkeley. Ellembergh, H., and Muel1er-Dombois, D. (1965). Tentative physiognomic-ecologieal c1assificaLion of plant Cormations of the hearth. Ber. Geobot. Inst. ETH, Sliflg Rubel Zurich, 37: 22-47. Garcia, J. E. (1988). Patrones Etologicos y Ecologicos del Mono Nocturno, Aotus azarae boliviensis, Ph.D. thesis, University oC Valencia, Spain. Garcia, J. E., and Braza, E (1987). ActiviLy rhythms and use oC space of a group of Aotus azarae in Bolivia during the rainy season. Primates, 28: 337-342. Hershkovitz, P. (1983). Two new species of night monkeys, genus Aotus (Cebidae, Platyrrhini): A preliminary report on Aotus taxonomy. Am. J. Primalol. 4; 209-243. Kinzey, W. G. (1981). The titi monkeys, genus Callicebus. In Coimbra-Filho, A. F., and Miltermeier, R. A. (eds.), Ecology and Behal/ior 01 Neotropical Primates, Vol. 1, Acad. Bras. Cien., Rio de Janeiro, pp. 241-273. Kinzey. W. G., Rosenberger, A. L., Heisler, P. S., Prowse, D. L., and Trilling, J. L. (1977). A preliminary Cield investigation of Lhe yellow handed titi monkey, Callicebus torqualUs torqualus. in norlhern Peru. Primates 18: 159-181. Lawick-Goodall, J. van. (1971). In the Shadow 01 Man, William Collins Sons, Glasglow. Liberman, M. (1985). Mapa de la Vegetacion: Estacion Biologica Beni, Laboratorio de CarLografia y Fotointerpretacion, Instituto de Ecologia, La Paz, Bolivia. Mason, W. A. (1966). Social organization oC lhe south American monkey, Callicebus moloch: A preliminary reporL Tulane Stud. Zool. 13: 23·28. Mason, W. A. (1968). Use oC space by Callicebus groups. In Jay, P. (ed.), Pn'mates: SlUdies in Adap/a/ion and Variability, Holt, Rinehart and Winston, New York, pp. 200-216. Maleucci, S. D., and Colma, A. (1982). Melodologia para el Estudio de la Vegetacion. Secretaria General de la Organizacion de Estados Americanos. Sen'e Biologia Monografia 22: 1- 168. Napier, E, and Napier, P. A. (1967). A Handbook 01 Lil/ing Primales, Academic Press, London. Ralhbun, G. B., and Gache, M. J. (1977). The S/atus 01 AoLus trivirgatus in Argentina, Centro Argenlino de Primates y el Instituto Nacional de la Salud, Washington, D. C. Schaller, G. B. (1964). The Year 01 the Gorilla, University of Chicago Press, Chicago. Terjung, W. H. (1966). Physiologic c1imates of the colerminous Uniled Statcs: A bioclimatic c1assificalion based on mano Ann. Am. Geog. Assoc. 16: 141-176. Sleeplng Sites Bnd Lodge Trees of lhe Nlght Monkey 477
Thorington, R. W., Jr., Muckenhirn, N. A., and Montgomery, G. G. (1976). Movements oC wild night monkey Aotus lrivirgatus. In Thorington, R. W., Jr., and Heltne, P. G. (eds.), Neotropical Primales, Nall. Acad. Sci. Washington, D.C., pp. 32-34. Wright, P. C. (1978). Home range, activity paLlern and agonistic encounters oC a group oC night monkeys (Aotus trivirgatus) in Peru. Folia Primalol. 29: 43-55. Wright, P. C. (1981). The night monkeys, genus Aolus. In Coimbra-Filho, A. F., and Mittermeier, R. A. (eds.), Ecology and Behavior o[ Neotropical Primates, VoL 1, Acad. Bras. Cien., Rio de Janeiro, pp. 2]]-240. Wright, P. C. (1983). Day-active night monkeys (Aotus trivirgatus) in lhe Chaco oC Paraguay Am. J. Phys. Anlhropol. 60(2): 272.